Lessons from the study of plant mating systems for exploring the causes and consequences of inbreeding in marine invertebrates

Many benthic marine invertebrates resemble plants in being modular and either sessile or sedentary, and by relying on an external vector to disperse their gametes. These shared features, along with recent evidence of inbreeding in these taxa, suggest that theory and practice bearing on the evolutionary costs and benefits of inbreeding for plants could advance our understanding of the ecology and evolution of invertebrate animals. We describe how the theory for the evolution of inbreeding and outbreeding could apply to benthic invertebrates, identify and compare techniques used to quantify inbreeding in plants and animals, translate relevant botanical concepts and empirical patterns to their zoological equivalents, and articulate predictions for how inbreeding might be associated with major axes of variation in sessile and sedentary marine invertebrates. The theory of inbreeding and outbreeding provides critical insight into major patterns of life-history variation in plants and holds similar promise as a complementary perspective on the evolution of reproductive traits, lifespan, ecological strategies, and dispersal in marine invertebrates. Extending what we have learned from plants to marine invertebrates promises to broaden the general study of mating systems.

Cytonuclear Genetic Incompatibilities in Plant Speciation

Due to the endosymbiotic origin of organelles, a pattern of coevolution and coadaptation between organellar and nuclear genomes is required for proper cell function. In this review, we focus on the impact of cytonuclear interaction on the reproductive isolation of plant species. We give examples of cases where species exhibit barriers to reproduction which involve plastid-nuclear or mito-nuclear genetic incompatibilities, and describe the evolutionary processes at play. We also discuss potential mechanisms of hybrid fitness recovery such as paternal leakage. Finally, we point out the possible interplay between plant mating systems and cytonuclear coevolution, and its consequence on plant speciation.

Ant guards influence the mating system of their plant hosts by altering pollinator behaviour

Ant guards can increase plant fitness by deterring herbivores but may also reduce it by interfering with pollination, hence ant-plant interactions are ideal systems in which to study costs and benefits of mutualisms. While ant impacts on herbivory are well-studied, much less is known about impacts on pollinators and associated consequences for plant mating systems and fitness. We used field experiments to quantify the effect of ant guards on pollinator community composition, frequency and duration of flower visits, and cascading effects on plant mating system and plant fitness in Turnera velutina (Passifloraceae). Although ant patrolling did not affect pollinator community composition or visitation frequency, it decreased pollinator foraging time and flower visit duration. Such behavioural changes resulted in reduced pollen deposition on stigmas, decreasing male fitness whilst increasing outcrossing rates. This study contributes to understanding how non-pollinators, such as these defensive mutualists, can shape plant mating systems.

Mating strategies dictate the importance of insect visits to native plants in urban fragments

Plant species conservation relies on their reproductive success and likelihood of population persistence. Knowledge of plant mating systems, particularly the relationship between plants and their pollinators, is fundamental to inform conservation efforts. This knowledge could be critical for prioritising efforts in human-dominated fragmented landscapes such as the world’s biodiversity hotspots, where reproductive success can be compromised due to habitat loss, limited access to pollinators or other factors. Yet, fundamental data on plant mating systems are lacking for many Australian plants. Here we determined the mating systems of native plant species growing in native woodland fragments within Perth’s urban landscape in south-western Australia. We manipulated insect access to flowers and pollen transfer on five locally common native species, then observed floral visitors and examined reproductive success. Hemiandra pungens and Patersonia occidentalis had mixed mating systems with some ability to self-pollinate, whereas Dianella revoluta and Jacksonia sericea were reliant on insects for outcross pollination. The fruits and seeds produced by Tricoryne elatior were too low to draw conclusions about its mating system. The introduced honey bee (Apis mellifera) was the sole visitor to the mixed mating species, whereas native bees visited D. revoluta and J. sericea (one bee species each). Overall, our data suggest that D. revoluta and J. sericea are more vulnerable to fragmentation than H. pungens and P. occidentalis. Although insects contributed significantly to the reproductive output of the two former plant species, our observations suggested low frequency and richness of insect visitors to these urban fragments. More research is required to determine the generality of our findings. A comparative study in larger native woodland fragments would help estimate the effect of fragmentation on insect pollinators and consequences for the insect-reliant plant species.

Geographic variation in reproductive assurance of Clarkia pulchella

Climate can affect plant populations through direct effects on physiology and fitness, and through indirect effects on their relationships with pollinating mutualists. We therefore expect that geographic variation in climate might lead to variation in plant mating systems. Biogeographic processes, such as range expansion, can also contribute to geographic patterns in mating system traits. We manipulated pollinator access to plants in eight sites spanning the geographic range of Clarkia pulchella to investigate geographic and climatic drivers of fruit production and seed set in the absence of pollinators (reproductive assurance). We examined how reproductive assurance and fruit production varied with the position of sites within the range of the species and with temperature and precipitation. We found that reproductive assurance in C. pulchella was greatest in populations in the northern part of the species’ range, and was not well-explained by any of the climate variables that we considered. In the absence of pollinators, some populations of C. pulchella have the capacity to increase fruit production, perhaps through resource reallocation, but this response is climate-dependent. Pollinators are important for reproduction in this species, and recruitment is sensitive to seed input. The degree of autonomous self-pollination that is possible in populations of this mixed-mating species may be shaped by historic biogeographic processes or variation in plant and pollinator community composition rather than variation in climate.